The inevitable journey to being

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Cite this article: Russell MJ, Nitschke W,
Branscomb E. 2013 The inevitable journey to
being. Phil Trans R Soc B 368: 20120254.
http://dx.d 0 i. 0 rg/l 0.1 098/rstb.201 2.0254

One contribution of 14 to a Discussion Meeting
Issue 'Energy transduction and genome
function: an evolutionary synthesis'.

Subject Areas:

biochemistry

Keywords:

origin of life, carbon fixation, alkaline
hydrothermal, disequilibria, pyrophosphatase

Author for correspondence:

Michael J. Russell

e-mail: michael.j.russell@jpl.nasa.gov

Royal Society Publishing

Informing the science
of the future

The inevitable journey to being

Michael J. Russell 1 , Wolfgang Nitschke 2 and Elbert Branscomb 3

Planetary Science Section 3225, MS:183-301, Jet Propulsion Laboratory, California Institute of Technology,
4800 Oak Grove Drive, Pasadena, CA 91109-8099, USA

2 Bioenergetique et Ingenierie des Proteines (UMR7281), CNRS/AMU, FR3479, Marseille, France
institute for Genomic Biology, University of Illinois, Urbana-Champaign, IL 61801, USA

Life is evolutionarily the most complex of the emergent symmetry-break-
ing, macroscopically organized dynamic structures in the Universe.
Members of this cascading series of disequilibria-converting systems, or
engines in Cottrell's terminology, become ever more complicated — more
chemical and less physical — as each engine extracts, exploits and generates
ever lower grades of energy and resources in the service of entropy gener-
ation. Each one of these engines emerges spontaneously from order created
by a particular mother engine or engines, as the disequilibrated potential
daughter is driven beyond a critical point. Exothermic serpentinization of
ocean crust is life's mother engine. It drives alkaline hydrothermal convec-
tion and thereby the spontaneous production of precipitated submarine
hydrothermal mounds. Here, the two chemical disequilibria directly causa-
tive in the emergence of life spontaneously arose across the mineral
precipitate membranes separating the acidulous, nitrate-bearing C0 2 -rich,
Hadean sea from the alkaline and CH 4 /H 2 -rich serpentinization-generated
effluents. Essential redox gradients — involving hydrothermal CH 4 and
H 2 as electron donors, C0 2 and nitrate, nitrite, and ferric iron from the
ambient ocean as acceptors — were imposed which functioned as the
original 'carbon-fixing engine'. At the same time, a post-critical-point
(milli)voltage pH potential (proton concentration gradient) drove the
condensation of orthophosphate to produce a high energy currency: 'the
pyrophosphatase engine'.

The general struggle for existence of animate beings is therefore not a struggle for raw
materials — these, for organisms, are air, water and soil, all abundantly available — nor
for energy which exists in plenty in any body in the form of heat . . . , but a struggle for
entropy [1]

1. The self-organizing universe

Given the extraordinary success of molecular genetics these days, it seems bad
form, not to say ignorant, to consider the emergence of life in terms other than
of the RNA world. However, the obvious need to drive inherently endergonic
chemical processes and sustain far from equilibrium states, not least to get a me-
tabolizing system going to manufacture the nucleotides in the first place, casts
doubt on such molecular vitalism. Of course, encouraged by the myriad of abiotic
molecules dispersed throughout space and brought to the Earth as dust and in
carbonaceous chondrites or generated through lightning, one might consider
instead spontaneous generation from a prebiotic organic world. However, then,
one would have to (i) overcome the infamous dilution problem, (ii) deal with
the fact that the early atmosphere was relatively oxidized, (iii) explain how the
inept earliest cells gained their energy, nutrition and catalysts and how chemios-
mosis got started, and (iv) deny the plain force of Schrodinger's 1944 stricture
regarding 'an organism's astonishing gift ... of "drinking orderliness" from a
suitable environment' [2-4]. Indeed, the apparent reluctance to dismiss the
simple idea of the organic soup as the recipe for the origin of biochemistry puts
one in mind of how spontaneous creation held back the field of cell biology in
the two centuries between van Leeuwenhoek and Pasteur [5]. Instead, an over-
arching theory for life's emergence is clearly required, one which first of all

© 2013 The Author(s) Published by the Royal Society. All rights reserved.

takes properly into account the thermodynamic requirements
inherent in the so-called order-creating processes, those med-
iating the first steps in the emergence of life in particular, and
second takes appropriate advantage of the torrent of new per-
tinent information pouring out of both the life, and the earth
sciences.

To this end, we first place the emergence of life in its full
context of the order-creating processes operating in the Uni-
verse. Our point of departure is this remark taken from
Kondepudi & Prigogine [6, p. 427]: 'One of the most pro-
found lessons of nonequilibrium thermodynamics is the
dual role of irreversible processes: as destroyers of order
near equilibrium and as creators of order far from equili-
brium'. And we begin by noting two key points about this
observation. First, for an irreversible process to be maintained
within a system, it must be embedded in, and exchange
energy and/or material with, a larger system that is itself in
disequilibrium, i.e. itself is ordered. Further, the embedding
must be such that the overall system frustrates to some
extent the flows acting to dissipate that embedding disequi-
librium. Therefore, an externally imposed order, one whose
dissipation is significantly frustrated, is needed to drive a
system into disequilibrium, and potentially far enough from
equilibrium that order-creating irreversible processes will
arise within it. In other words, it takes (the dissipation of)
order to create order. Second, the order that arises in this
way is always an engine — an engine that acts to accelerate
the dissipation of the disequilibrium that drove it into exist-
ence in the first place and upon which it feeds [7]. As such
it is driven by a greater entropy-producing flow that is dissi-
pating the embedding disequilibrium and producing work
in the form of a lesser entropy-consuming, i.e. order-creating,
flow. Engines are thus disequilibrium converters, or in more
conventional terms, free energy converters. Furthermore, and
critically, such engines are always autocatalytic, either
directly or indirectly; made so by the fact that the work
they produce acts back on the engine with the effect of
increasing its throughput and stabilizing it against decay
[8]. It is because of this positive feedback that the engines
are emergent, and self-organizing, and it is through the
resultant autocatalytic growth, that they accelerate the rate
at which the driving disequilibrium is dissipated. Thus,
there is the paradoxical fact that far-from-equilibrium order,
in its haste to be dissipated, is compelled to create order —
in the form of engines of dissipation — that it might accelerate
its dissipation. All order in our present universe is presum-
ably born of this paradox. Order, therefore, is inherently
dynamic, transient and hierarchical and — in obedience to
the second-law's diktat that all change must increase the
entropy of the universe — serves to quicken that increase
through the concomitant destruction of order by the transient
creation of order.

Indeed, this has been the business of our Universe since its
birthing in the Big Bang — the initial condition — at which
moment it stood at an almost unimaginable distance from equi-
librium, and thus in a state of nearly infinite thermo dynamic
stress [9-12]. Its evolution since has been solely about dissipat-
ing that disequilibrium at the maximum achievable rate. This it
has done, and is doing, largely by creating order in the form of
engines of dissipation — of emergent, self-organizing, autocata-
lytic engines, as we noted earlier, whose thermodynamic raison
d'etre is to open and/ or widen the channels of dissipation that
mediate the relaxation of the particular disequilibrium that

gave each its birth and upon which it feeds [7]. However, each
such engine does only a small part of the total job and
each itself is, and creates, a new disequilibrium — a new ordered
state — which, in turn, induces the creation of subordinate engines
to devour and dissipate it, as we noted earlier. The vast industry
of cascading dissipation-accelerating engines that emerge
in this circumstance forms a great, evolving, self-organizing,
dynamic web.

Our particular concern here is to demonstrate how life is a
natural and expected outcome of thermodynamically driven
order creation through symmetry-breaking in our far-from-
equilibrium Universe. To this end, it is helpful to have a
clear understanding of what is required to give birth to a dis-
sipative engine, and as part of that what controls the
transition between order-destroying and order-creating dissi-
pative processes as referred to in the earlier-mentioned quote
from Kondepudi & Prigogine [6]. For this, we need to delve a
bit into the theory of non-equilibrium thermodynamics and
open systems — a theory largely initiated by Onsager [13]
who analysed the near-equilibrium realm, but which received
its original general development at the hands of several
investigators, including De Groot & Mazur [14], Jou et al.
[15] and Prigogine [16] (together with his co-investigators;
principally Glandsdorff & Nicolis [17,18]).

Such systems, Prigogine first argued, go through qualita-
tively distinct phases as a function of how far from
equilibrium they are driven. In the near-equilibrium region,
which Prigogine called the thermodynamic branch [16-18],
the thermodynamic forces induced by the free energy influx
give rise to fluxes which (i) are proportional to the forces
and, most importantly, (ii) respect the symmetries that
characterize the system at equilibrium. That is, the dissipative
fluxes induced in this branch do not involve macroscopic
organization, and thus have the same high spatial and tem-
poral symmetry of the equilibrium state. Furthermore, the
flows induced in this realm are stable dynamic states in that
the system responds to perturbative fluctuations by damping
them out exponentially. Thermal conduction is an example.
As the system is driven further from equilibrium by increasing
the strength of the free energy influx, a critical point is reached
(the bifurcation point) at which this equilibrium-like dynamical
behaviour is no longer stable, and the system responds to
perturbing fluctuations by diverging into a new state which
is (i) stable to perturbations in the post-bifurcation region,
(ii) does not honour all of the symmetries of the equilibrium
state (i.e. symmetry breaking), and (iii) is symmetry breaking
because it involves flows and structures that are macroscopic-
ally organized; that is they have structure at the macroscopic
scale — convection cells being the graphic example as we shall
investigate in §4. Such organized dynamic states are called
dissipative structures by Prigogine and are inherently low
entropy and are therefore, inherently unstable and transient
forms of matter.

It is important to note that these self-organizing dissipa-
tive structures are free-energy-converting (FEC) mechanisms;
as noted earlier, they tie together a free-energy-consuming
flow and a free-energy-generating one — as the engine's
work output — into a single, indivisible and spontaneous ther-
modynamic process. Cottrell [7] has aptly identified these
structures as engines. However, as was also noted earlier,
they are in addition quite phenomenal engines in being,
either directly or indirectly, autocatalytic (not only do they
corral the energetic and material output from a preceding

rstb.royalsocietypublishing.org Phil Trans R Soc B 368: 20120254

engine, but also consume the disequilibrium free energy they
produce as engines to maintain and grow themselves). And
we may take Cottrell's exegesis on Prigogine's argument [7]
to further imply that all macroscopically organized non-
equilibrium arrangements of matter and energy owe their
existence to the kind of far-from-equilibrium self-organizing,
FEC engines described by him.

However, to this general picture, Cottrell has added an
important qualification — namely that not all naturally arising
FEC engines need generate from scratch and by themselves
their own broken symmetry-organized structures that can
operate as their coupling device. In some cases, the structures
are already present — at least in a form sufficient to seed, or
template the autocatalytic growth of a new engine — and are
present as the by-product of the operation of independent
and in general unrelated dissipative engines. In these cases,
driving gradients of relatively modest strength can be sufficient
to initiate dissipative engines and keep them fed and growing.
An example of this as it applies to the emergence of life are
the inorganic prebiotic mineral structures involving iron
sulfides, dosed with nickel, cobalt and molybdenum and
the iron oxyhydroxides, so similar to the active centres of the
metalloenzymes, that played a vital role in the first metabolic
pathways [19-21].

Therefore, in our search for the FEC engines that would
have been required to energize the emergence of life, we
need to keep in mind both ways in which such engines can
arise. And it is clear that in broad strokes, the dissipation hier-
archy taking us from geological dissipation to life is very likely
to have been a mix of both types — and possibly indeed of
hybrid types. Furthermore, embedded in this dissipation
typology is the profoundly important distinction between —
and transition between — primarily physical and primarily
chemical dissipative engines. It is clear that various types of
engines, drawn from this palette of options and driven in
series, are involved, and culminate in, life's emergence: in the
terminal steps in the cascade set in motion by the Big Bang;
these include gravitational accretion, tectonic convection, ser-
pentinization and the chemical free energy conversions of
proto-metabolism to hit just a few high points [22-27]. Although
the primary engines in this hierarchy are essentially large and
physical, i.e. solar system and planetary accretion and then
whole body thermal convection in the mantle; downstream the
engines are hybrids, involving ever more chemical and even-
tually electrochemical energies, whereas the newly emergent
physical mechanisms are nanometric. It is the coupling of
serpentinization, through hydrothermal convection, to the for-
mation of porous submarine mounds that is of most concern
here. Indeed, it is the serpentinization of peridotite — the mag-
nesium iron silicate comprising portions of the floor of both
the first ocean and parts of the ocean today — that offers us still
an observational gallery to the operations of life's parental
engine. We turn next to connecting the self-organizing dynamics
of the Universe as they act at the astrophysical scale to those
which produced the engines leading directly to life.

2. From astrophysical to terrestrial engines
of dissipation

It is ultimately the dynamics of the geometry of space -time
itself, which is to say the force of gravity, that has driven
the self-organization of the Universe which is everywhere

in the form of engines accelerating the dissipation of order.
That is, this great drama too is thermodynamic in nature
and its ultimate driver is the tendency of the curvature of
space -time, in the presence of distributions of mass, to
increase locally, and grow more complex, more entropic,
with time [12].

As this implies, gravitational collapse is, counterintuitively,
a second-law-abiding, entropy-producing process, one whose
limit (albeit a transient one — if trillions of years counts for
transiency [11]) is the black hole state in which the entropy
per unit mass (and the curvature of space -time) is maximal
[22]. Importantly, however, reaching that maximum is a
remote and frustrated — and potentially even futile — dream
for much of the mass of the Universe. Impeding the way are
a variety of obstacles [28, ch. 4]. Two have particular relevance
to the emergence of life. First, the conservation of angular
momentum obliges all gravitational collapse not proceeding
from a state of near-perfect spherical symmetry to go no
farther, initially, than into the formation of vast spinning vor-
tices; vortices that fragment into hierarchies of lesser vortices.
At this hierarchy's top stand giant assemblies of galactic clus-
ters, each cluster containing immense inventories of galaxies,
each of these with immense inventories of stars (not to mention
many other forms of matter and energy). All these dynamic
structures too are engines of dissipation, albeit engines that
grind exceedingly fine. Second, there is the obstacle of nuclear
fusion, which postpones further collapse of star-sized clumps,
while providing the FEC engines of greatest direct relevance to
the existence of life, until, that is, the hydrogen endowment of
each has been consumed and its fire dies. Providentially, of
course, more massive stars are shorter lived, and in their
necessarily unpeaceful deaths bequeath to their cosmic neigh-
bourhoods all nuclei beyond lithium — and thereby make it
possible for subsequently formed stars to host wet, rocky
planets; rocky planets most vitally with a healthy endowment
of radionuclides bearing billion-year half-lives — sufficient, that
is, to keep a rocky planet of good size in a tectonic boil — at least
for the time required for the fledgling of life to take wing on the
updrafts from serpentinization, taking advantage as it does of
those other trans-lithium elements for catalysis all the way up
to atomic number 74, tungsten [20]. In any case, it is in the
accretion of rocky planets that the Universe's cascade of
engines finally descends to the point where the order produced
directly sets the table for the emergence of life [29]. But how
that table is set depends on just how the accretion process
takes place.

In detail, planetary accretion proceeds through runaway
growth of ever larger wet rocky bodies comprising magnesium
silicates and nickel iron bodies, comets and carbonaceous chon-
drites, though collisional erosion is also involved [30-32]. Once
the rocky bodies have the dimensions approaching our Moon,
such planetesimals collide to produce the terrestrial planets
[32]. Primeval gases still surrounding these proximal planets
are blown outward by solar winds beyond the so-called snow-
line to the colder reaches of the system [33-35]. The chemical
and mineralogical composition of rocky bodies depends on
the make-up of the protoplanetary disc. For example, those
with a carbon : oxygen ratio twice that of our Solar System
would produce dry and lifeless silicon carbide planets
[36,37]. In our own system, carbonaceous chondrites merely
added to the carbon budget of the wet siliceous rocky planets
and the moons of Jupiter and Saturn, bom as it was of multiple
supernova explosions [11,38]. The chemical composition of the

rstb.royalsocietypublishing.org Phil Trans R Soc B 368: 20120254

gases that remained dissolved in our own planet's hot interior
was controlled by its mineralogical composition — in particular
of iron [3].

Once the Earth reached a critical size, gravitational and
radiogenic heat melted the heterogeneous mantle accreted
from dense native iron and less dense silicates. The larger
iron bodies would have sunk towards the centre of our spin-
ning world, dissolving dense blobs as they did so, picking up
speed and dragging more in their wakes, generating even
more heat until landing in, and as, the core. The remaining
ferrous iron then self-oxidized to the smaller ferric iron
under these high pressures and partitioned into the alumin-
ous silicate perovskite fraction (approx. A1 2 0 3 ), the
dominant mineral in the lower mantle [39,40]:

3Fe n O + A1 2 0 3 -> 2Fe m A10 3 + Fe°|, (2.1)

while the native iron fraction left over joined the gravitational
scramble to the core. This reaction left the mantle with a sur-
prisingly low hydrogen fugacity (i.e. a relatively high oxygen
fugacity) such that the state of carbon dissolved or present in
the mantle was as its oxide (figure 1) [41].

Thus, the fate of carbon in the early Earth was to be oxi-
dized to carbonate or carbon dioxide within the first 100 Myr
[42]. The upshot was that volcanoes dispensed great volumes
of C0 2 to the early atmosphere as Darwin [47], Haeckel [48],
Mereschkowsky [49] and Leduc [50] had surmised. Indeed, a
pressure of 10 bar or more was likely at least at times when
carbonated ocean floor was reheated in mantle down-
draughts and the gas returned to the atmosphere [42,43].
Hydrogen too was essentially oxidized at these high tempera-
tures to water vapour, and it too was exhaled to produce the
all-enveloping universal carbonic ocean perhaps 8 km or so
deep [51,52]. Other oxidized volatiles were pyrophosphate,
nitric oxide and sulfur dioxide [53-56].

3. Driving for life: convective engines

The gravitational and radiogenic heating of the Earth's rocks
generated a gravitationally orientated thermal gradient that
exceeded the Rayleigh limit and therefore (as prescribed by
Prigogine) gave rise within the mantle to organized, auto-
catalytic convective engines of dissipation. It is, of course,
to these engines that we ultimately owe the creative, far-from-
equilibrium tectonic dynamism of our planet. In turn, these
convective flows both drove and were accelerated by another
self-organizing dynamics to which they were coupled, namely
density-dependent chemical fractionation — fractionation be-
tween relatively buoyant magnesium-silicate-rich minerals
that became enriched in the upper mantle, and denser, native
iron masses and globules preferentially relegated to the core.
The resulting, continuously refreshed, mineralogical organiza-
tion of the planet, whose mechanistic details we review next,
was no less essential to its ability to spawn life.

As gravitational energy drove the differentiation of the
iron core, conversely the relatively buoyant, magnesium-sili-
cate-rich upper mantle began to rise differentially upward.
Whether in the Hadean, these mass transfer convective
flows were in well-organized convection cells as they are
now and thereby drove conventional plate tectonic activity
or were less organized and mainly involved mantle plumes
is much disputed [27,57]. Whichever the dominant form,
it was inevitable that ocean floor would have been

Figure 1 . The oxidation state of the upper mantle 100 Myr after its for-
mation was controlled by the quartz/magnetite/fayalite buffer (QFM =
Si 0 2 /Fe 2 Si 0 4 /Fe ll Fe 2 l 04 ) [3,40,42]. The dominant state of carbon in the
upper mantle was as its full oxide with vanishingly small concentrations
of methane (black diamonds) [41], explaining why the early atmosphere,
mainly supplied by volcanoes, was dominated by C0 2 along with nitrogen
and lesser S0 2 and NO. However, as shown by Shock [43], there is a
cross-over of the oxidation states of carbon and iron very approximately at
around 400°C. At the lower temperatures towards and at the surface of
our planet the equilibrium state is methane (grey diamonds) as produced
in hydrothermal systems through serpentinization [44,45], though the abiotic
reduction of C0 2 at the Earth's surface is thermodynamically challenged. It is
this metastable field (grey diamonds) that Shock [43] termed 'the locus of
biochemistry within geochemistry'. However, iron minerals comprising the
QFM buffer would also tend to catalyse the reduction/hydrogenation of
C0 2 to formate and methane. A further buffer (PPM = pyrite/pyrrhotite/
magnetite or Fe M S 2 /Feo ^sS/Fe’^e^OJ operating where sulfide is concen-
trated would also tend to control the oxidation state of carbon at lower
hydrogen fugacities and might be expected to catalyse redox reactions.
The even more oxidized HM buffer (haematite/magnetite or Fe^/F^Fe"^)
would be comparable to the mixed valence mineral green rust (e.g.
[Fe ll Fe lll (0H) 4 ] + [0H] - ) which might oxidize methane to organic intermedi-
ates at temperatures around 40°C [46]. Note how the redox state of iron
contributes to the geochemical conditions that drove life into being and
thereafter was central to its further evolution. Based on Shock [43].

continually renewed. Holmes [58] was first to provide a
viable mechanism for the formation of new ocean floor for-
mation as an aspect of thermal convection of the Earth's
mantle not restricted merely to reliance on buoyant mantle
updraughts. His mechanism involved a catalytic feedback
caused by a mineralogical phase change, one induced by
pressure so that the density of the now cool, down-welling
limb continuously increased, pulling the advecting ocean
floor behind it, so acting in concert with the push from the
rising limb. The phase change involved olivine, pyroxene
and feldspar, with a density of approximately 3.0 kg dm -3 ,
that metamorphosed to eclogite (a garnet pyroxene rock)
with a density of approximately 3.5 kg dm -3 , so providing

rstb.royalsocietypublishing.org Phil Trans R Soc B 368: 20120254

;ic dykes and flows
400°C springs^^

ocean

crust

granodiorite

C0 2 > N 2 > H 2 0 > S0 2 > CO > NO > h 2 s ~h 2 ?

calc-alkaline

propagating warm
alkaline seepage

magmatism

C0 2 traceof

atmosphere

basaltic

spreading

centre

410°C springs

obduction and
sagduction

sulhde mound

oceans

oceanic

ocean

source

of

komatiitic

magma

■ eclogite
p= 3.5

eclogite
I p= 3.5
^ peridotites
sulfides

mantle convection I k
engine at 4.4 Ga

basalt
magma
p= 2.8

i Fe(Ni)S
melts

‘ U' ' ) ' ) k v n

i / upper mantle i

lower mantle

Figure 2. Diagram to show how a mantle convection engine continually provided new and reactive ocean floor in the Hadean as well as oxidized volatiles to feed
the hydrosphere and atmosphere [24,27]. Hot buoyant updraughts of partially molten mantle transfer heat to the surface, so dividing and pushing the ocean floor
apart. At the same time, a density inversion drives the basalt-to-edogite transition which, in turn, produced further gravitational energy to the downward-pulling
limbs with friction regulating flow rate [58]. Thick ocean lava plateaus were another result of mass transfer of heat in mantle plumes towards the Earth's surface. The
atmosphere was relatively oxidized though the proportions of its components are not well constrained [3,42,52,55]. The figure provides a framework in which to
understand the chemical and thermal energies produced in such an environment from submarine water- rock interactions that drove anaerobic litho-chemosynthetic
life into being in a submarine hatchery around 4.4 Ga. It took more than another billion and a half years for wide littoral continental areas to develop and provide a
nursery for burgeoning oxygenic photosynthesizers around 2.7 Ga [25,61-63]. Adapted from Russell et al. [24].

the body force to help drive this engine. Such a process might
be expected to have operated with even more vigour in the
Hadean when the oceanic crust was richer in olivine and
the temperature of the mantle was perhaps 200° C hotter
than it is today [59,60].

We have adopted a similar ocean floor spreading mechan-
ism to explain the continual renewal of ocean floor in the
Hadean driven by just the catalytic feedback mechanism
envisaged by Holmes but with the added contribution of
magmatic plumes rising vertically from the core mantle
boundary [27,30,57,58] (figure 2). Bedard [64] has suggested
that such vertical tectonics would also involve the transition
to dense eclogite in a catalytic mechanism involving delamin-
ation of the lower crust whereby the descending eclogite
would guide repeated updraughts of mantle material while
at the same time augmenting the differentiation of silicate
magmas to produce high temperature submarine hydrother-
mal exhalations (cf. [65]). These exhalations would help
provide the trace elements to the ocean required of life's
inorganic catalysts as described in §§4 and 5 [25,61].

4. Serpentinization: life's mother engine

One effect of mantle convection is to stress the new and rela-
tively homogeneous oceanic crust beyond its elastic limit, i.e.
its brittle strength. Stresses may be tensional and/or com-
pressional. Given the irregular textures of the magnesium +
iron + (alumina)-silicate lavas such as komatiite and basalt.

and magmatic intrusions such as peridotite or gabbro com-
prising the early ocean floor, any resulting fractures that
penetrate the surface will tend to be somewhat irregular,
thus increasing permeability and allowing access to ocean
water which then gravitates to depth. Again, a positive feed-
back is realized in that the hydrostatic pore pressure increases
the effective stress such that the fractures tend to extend. Frac-
turing loads the next weakness which then fractures in turn.
Or rupturing is prevented by a mineral knot and stress
accumulates which has to find a new weak zone of fracture
[66]. Hydration locally increases rock volume, causing second-
ary stresses and strains. Thus, populations of reproducing
parallel, tensional or sheer and interleaving cracks and frac-
tures propagate as do secondary and tertiary fractures as
the stresses are modulated by newly formed free surfaces.
Elastic and chemical energies stored in crystals at the frac-
ture tips are transformed into surface free energy which, in
turn, is stored at the crystal surface at the breaking point of
imminent ductile to brittle rupture /failure during hydro-
fracturing [66-68]. This stored chemical energy may be
used to reduce the percolating water and carbon dioxide
to hydrogen, formate and methane as explained below [44].
In such a stressed system, the longer the fractures, the less
the energy required for their further extension and repro-
duction, i.e. they are autocatalytic [7]. The failure points
absorbing and converting the tectonic free energies are, more-
over, engines that can produce more engines [7]. Submarine
hydrothermal convection cells that serpentinize the crust in
this fashion and transfer heat to the ocean are of two main

rstb.royalsocietypublishing.org Phil Trans R Soc B 368: 20120254

types: (i) a hot (400°C and above) magma-driven system over
spreading centres and magmatic plumes and (ii) open system
non-magmatic convection cells (less than or equal to 150°C)
operating in the older, cooling crust away from such centres
(figure 2).

The first type of aqueous submarine convection cell, the
400°C and above cell forced by magmatic intrusion emerging
from the mantle convection engine or at magmatic plumes,
played merely the supporting role in the emergence of life of
loading the Hadean Ocean with catalytically potent transition
metals. The intrusion of magma caused tensional rifting,
especially at ocean spreading centres. Water gravitated down
these active rift faults until the pressure-dependent buoyancy
of magnesium-bearing salt water at its critical point at around
410°C drove the fluids back to the surface. At the critical temp-
erature these fluids were, and are, buffered to acidic pH as
magnesium silicate hydroxides are formed from the pyroxene
enstatite, with the generation of high temperature serpentinite
and the release of protons (figure 2) [61,69] (equation 4.1):

2M gSi0 3( ensta t i t e)+Mg 2+ +3H20

" Mg 3 Si 2 0 5 (0H) 4(serpentine) + 2H + . (4.1)

These acidic waters dissolved the transition metals (iron,
nickel, zinc, cobalt and tungsten) from the oceanic crust and
dispensed them to the carbonic Hadean Ocean where they
remained in often supersaturated solution until they met sub-
marine alkaline, moderate temperature springs. Thus, the
Hadean Ocean acted as an effective reserve for metal catalysts
for emergent life, and eventually for the active centres in
peptides and proteins [70-76]. We recognize these high temp-
erature systems today as the iconic black smokers — black
because unlike in the Hadean, the metals precipitate rapidly
on meeting alkaline oxidized ocean waters [77,78].

It is the second, lower temperature type of serpentinizing
system that operated away from magmatic intrusions that
bore most directly on the emergence of life [26,43]. The dis-
covery in the year 2000 of the so-called Lost City springs
15 km distant from the mid- Atlantic Ridge gave credence to
this hypothesis. Such hydrothermal convection cells operate
at a probable maximum temperature of 150°C [25,44,79-81]
and are driven by heat residing in the crust and by exothermic
reactions — a further example of an engine feeding off its own
output. A deeply penetrating near vertical fracture might well
have begun the process away from ocean spreading centres
[82]. The hydrothermal convection progresses through the
generation of cracks at scales ranging from kilometric to
nanometric, dominantly in response to tectonic stress at the
larger scales and through positive feedback involving
increases in pore pressure, chemical alteration and the force
of crystallization at the smaller scales, and finally through dif-
fusion in the rock matrix. Such feedbacks explain why the
Lost City hydrothermal system appears to have continued
operation for at least the past 30 000 years (or in more appro-
priate units for the emergent processes under consideration,
10 17 ps) [83]. The solutions produced in this process are
thermostated (approx, at 150°C) by the brittle-to-ductile tran-
sition through serpentinization, whereas their pH is buffered
to around 11 by the precipitation of magnesium hydroxide
(the mineral brucite), and some cations (mainly calcium) are
released to solution to balance charge [84,85]. At the same
time, ferrous iron in olivine reduces some of the water to

hydrogen as shown in this highly simplified reaction [85]:

3Mg 1 8 Fe 0 .2SiO4 (olivine) + 4.1H 2 0

-»■ 1.5Mg 3 Si 2 0 5 (0H) 4(serpentine) + 0.9Mg(OH) 2(brucite)

+ 0.2Fe3O4( ma g net it e ) + O. 2 H 2 T •

(4.2)

Similar reductions [86-88] are responsible for methane
generation from carbon dioxide idealized as:

6 Fe 2 Si 0 4 (fayalite olivine) 5“ ^~'^ 2 (aq) T 2 H 2 O

~ * 6Si02(quartz) + 4Fe30 4 + CH 4 t , (4.3)

and

24Fe2Si0 4 T 26H2O -I- C02(aq)

12Fe3Si205(0H) 4 ( greenalite ) + 4Fe30 4 + CH4 j . (4.4)

While these reactions progress rapidly at high temperatures
[89], the methane : hydrogen ratio increases at lower tempera-
tures as shown by Etiope et al. [90] using isotopic analyses of
carbon and hydrogen. Substantial methane emanating from
deeper within the crust is also added to the convecting solutions
from below [44,90-94] (figure 3). The methane, formate and
hydrogen emerging in the lower-temperature serpentinization
effluents then provide the electron-donor fuels offered at the
emergence of life. Other constituents released or generated
during lower-temperature serpentinization are bisulfide
(HS ), ammonia and molybdenum and tungsten as Mo IV /
W IV S/Se 3 _ x O*' orMo VI /W VI S/Se 4 _ x 0 7 “ [102-107].

A point to note here is that it is largely in the process of ser-
pentinization that the cascade of dissipation engines relieving
the Earth of its heat burden makes the fateful transition from
largely physical to largely chemical FEC engines. That is, the
serpentinization process primarily converts physical disequili-
bria, in the form of mechanical stress and thermal gradients, to
the production of structural, mineralogical, and most notably,
chemical disequilibria — all of which then serve to directly set
the table for the emergence of life.

5. The vehicle for the first metabolic free-
energy-converting engines: turnstiles and
electron bifurcators

Extant life works largely through the operations of remarkable
nano-devices [108], many of which are merely clever equilib-
rium mechanisms functioning as catalysts, switches and
passive carriers (e.g. haemoglobin [109], aconitase [110] and
Zflc-repressor [111]). However, those that mediate the critical,
but inherently non-equilibrium activity of free energy conver-
sion, i.e. function as engines, form a functionally distinct
class. And, because this is the class of nano-devices that con-
cern us here, and that we are seeking to find at work in the
dost cities' of the Hadean, we need to ask what sorts of nano-
device mechanisms are required to effect chemical free
energy conversion. Here, the picture is not entirely simple.
Most analysed examples of biological devices in the engine
class have proved to depend critically on physically moving
parts (cavities and passages that open and close, parts of pro-
teins that move relative to each other, etc.). These include,
redox-driven proton pumps [112], rotor- stator type ATPases
[113-115] and all other motors [116], and membrane-integral

rstb.royalsocietypublishing.org Phil Trans R Soc B 368: 20120254

4.4 Ga acidic ocean
~10°C pH~5.5

acetate

exhaust’

hydrothermal mound
= hatchery of life

electron sinks
CO 2 NO-NO-S0Fe 3+ Mn 4+

pH~5.5

nitrate electron
acceptor

ocean floor

ocean crust

serpentinization produces electron donors in alkaline hydrothermal fluid

^ ^ ^ ^ ^

chemical free energy (disequilibria) derived from serpentinization

the serpentinization engine
i.e. free energy, converter;

t

t t t

*

t t t

t

physical free energy from the mantle convection engine

*

Figure 3. The final cascade of engines leading to the emergence of life. The mantle convection engine (figure 2) delivers heat to the near surface and stresses the
crust to effectively feed the serpentinization engine. The photographic montage of a typical, scale invariant example of serpentinite, offers us a gallery view of the
composite engine responsible for driving life into being. The olivine-rich crustal rock fractures in response to the convective stress. The initial fractures propagate and
anastomose as carbonic ocean water gravitates to depth and interacts with the hot rock. The hydrodynamic pressure increases the effective stress while at the same
time exothermically oxidizing, carbonating, hydrating and hydrolysing the mineral constituents so allowing further access of water to rock. The force of crystallization
causes large-scale expansion of the rock body, further fracturing and lowering the density of the rock, leading to diapirism and yet further fracturing. Apart from the
physical free energy released as heat [95] by this disorganization, chemical free energy is also released, particularly at the propagating fracture tips. Here fresh iron —
nickel-bearing mineral surfaces reduce water to hydrogen, whereas carbon dioxide is reduced to formate and methane, fuels for emerging life [44,96-98]. At the
same time, calcium and some magnesium and sulfide ions are released to the fluids rendering them highly alkaline. Temperature is regulated by rock strength at
the base of the cell while pH is buffered to approximately 11 units by brucite (Mg(0H) 2 ). This well-ordered hydrothermal effluent is driven convectively to the ocean
floor where, on interaction with mildly acidic ocean water, porous mounds comprising iron -magnesium hydroxides and silicates, iron -nickel -cobalt -molybdenum
sulfides and ephemeral iron -calcium -magnesium carbonates are precipitated [24,25,99]. We argue here that some of the marginal compartments, subjected to
redox, pH and thermal gradients, assemble natural engines to dissipate these disequilibria while driving endergonic (anti-entropic) reactions: (i) a nickel/iron/mo-
lybdenum sulfide engine reducing C0 2 to CO, (ii) an electron bifurcating mixed valence molybdenum-bearing iron sulfide composite engine dissipates redox energy
through the reduction of nitrite while oxidizing hydrothermal methane and reducing oceanic carbon dioxide, resulting in the generation of activated acetate [46],
(iii) a pyrophosphatase engine comprising green rust interlayers [100,101] that clamp contiguous orthophosphates (2 x HPO 4 - or Pi 2- ) in a natural metal ion
mediated binding site where they condense, only to be released in the proton flux [19].

pyrophosphatases [117-119]. On the other hand, such moving-
parts mechanisms are not inherently required for chemical free
energy conversion and, as we argue here, may well not be
directly involved in electron-bifurcation — one of the two
classes of FEC devices that we here propose got life started.
Even in that case, however, moving parts mechanisms may
have had a role to play which is not unlike the role they have
been seen to play in the analysed examples of electron bifurcat-
ing engines, such as the Q-cycle protein complex [120].
Furthermore, the other class of FEC devices which we believe
was necessary for life's emergence does appear to inherently
require moving parts mechanisms as we discuss below.
These considerations argue strongly that if we must identify
abiotic devices that could serve as the first engines of chemical
free energy conversion to power, the first steps in the launching
of life, then they will likely be found in physical settings
that could provide, among other things, the right kind of
controllable physical flexibility and movable parts.

But finding such devices in an abiotic world seems a
daunting challenge, so it is worth pausing to ask whether
this is really one we have to take on. Is the right model of
the emergence of life an 'engines-first' one; that is, do we
really need FEC engines, as we are here supposing, just to
initiate the very first steps in the transition to life? And
then if we do, is it really feasible that the mineralogical con-
structions within the alkaline hydrothermal mounds could
provide the controllable moving parts that most, if not all,
biologically relevant chemical free energy conversion seems
to require?

As to the first point, the fact that all extant life is, and
inherently depends on being, a far-from-equilibrium physical
system, in both structure and process, makes it hard to
believe that it could ever have been otherwise. However, in
the production and maintenance of this far-from-equilibrium
system, the second law requires that life is essentially a con-
struct of FEC engines — all the way up as well as all the

rstb.royalsocietypublishing.org Phil Trans R Soc B 368: 20120254

way down. These considerations support the proposition that
FEC engines were the essential enabling inventions at life's
very onset, although this is admittedly not the general view
of the matter. The question, of course, comes down to whether
life can begin exclusively with chemistry operating at (or very
near) equilibrium. If the answer is no, then some reactions must
be driving significantly away from equilibrium, driven, that is,
in spite of being endergonic, and this, by the second law, ines-
capably requires that they be coupled to a thermodynamically
larger exergonic reaction via an FEC engine.

If we need, for example, an ATP-like diffusible source of
free energy at the start, such as would be provided by pyro-
phosphate in disequilibrium with respect to its hydrolysis
products, then we inescapably need to have that disequilib-
rium produced (and maintained) by being coupled to some
external source of free energy via an engine (note that it is
the posited disequilibrium that alone makes pyrophosphate —
or anything else — a source of free energy for driving other
reactions; pyrophosphate at equilibrium with its hydrolysis
products, no matter its concentration, is exactly useless as a
source of driving free energy). Or if we need, at the start,
some form of fixed carbon at levels above equilibrium with
its oxidation products, or produced by a path that involves
an endergonic step, then we again must find an engine that
can couple these anti-entropic processes to a driving source
of free energy. Equilibrium chemistry, no matter how facili-
tated by catalysts, or shifted by the manipulation of reactant
concentrations, is prevented in principle from filling this bill.
That is, if proto-life requires any non-equilibrium states to be
maintained, as we argue here, then it must have invented
true engines for the purpose that were fed by the geochemically
given sources of free energy (disequilibria) and which had
as their work output the needed non-equilibrium states
[8,46,121]. For this purpose then, toying with the thermo-
dynamic parameters of simple equilibrium reactions,
whatever the context, is not going to help. Instead, we argue,
FEC engines, including both chemiosmotic and electron bifur-
cating engines, coming into play right at life's emergence — if
only we could divine how they might have done so — would
explain how the essential, but thermodynamically anti-entro-
pic first steps (i) to carbon dioxide reduction via exergonic
steps, (ii) methane oxidation, and (iii) phosphate condensation
being driven far from equilibrium with respect to phosphate,
could be made to happen. Given these three particular chal-
lenges, we first outline the hydrothermal environment,
vouchsafed by serpentinization, in which particular free
energy sources are on offer in the form of steep chemical,
redox, pH and thermal gradients. We later return to the ques-
tion of whether the vent precipitates might provide the kind
of controllable flexibility devices that are found functioning
as the beating heart of nearly all extant biological FEC devices.

Upon exhalation, the alkaline and reduced hydrothermal
fluids at approximately 100°C interacted with the acidulous,
somewhat oxidized, ocean [122] to precipitate porous inor-
ganic mounds [123-125]. The main precipitates consisted of
silica, silicates, oxyhydroxides, phosphates and ephemeral
carbonates, and, in cases where bisulfide was exhaled,
metal sulfides (figure 4). Mixed valence iron (nickel) sul-
fides (mackinawite and the thiospinels, greigite and
violarite) and iron oxyhydroxides (green rust) dominated
the mineralogy [128-136]. It is worth noting in passing that
mackinawite, violarite and greigite have structures generally
affine with the active centres of hydrogenase (CO

dehydrogenase (CODH) and acetyl coenzyme-A synthase
(ACS)), whereas green rust has a similar structure to di-iron
methane monooxygenase [19,126,133-136].

In laboratory simulations, pore volumes of the inorganic
precipitates ranged between 10 and 1 ml, and the compart-
ment walls were from 4 to 100 pm thick (figure 4) [123].
The silica, calcium, magnesium, carbonate, phosphate and
most of the transition metals such as iron, nickel, cobalt,
zinc and tungsten making up these inorganic membranes
were contributed from the ocean, while sulfide, trace mol-
ybdenum (as MoO„S|l n ) and additional calcium,
magnesium and trace tungsten were carried in the alkaline
hydrothermal solution [25,71,81,103-105,122-125]. In their
various forms and compositions, the compartmentalized pre-
cipitates or bubble cells tended to keep the two contrasting
solutions apart and far from equilibrium. Steep chemical,
redox, pH and thermal gradients were imposed across the
inorganic membranes comprising the outermost compart-
ments of the hydrothermal mound. Iron was precipitated in
multiple distinct, chemically reactive forms, many of them of
mixed valence. Initially, these comprised ferrous iron as ephem-
eral siderite (Fe 2 C0 3 ), as ferrous hydroxide (Fe(OH) 2 ) and
mackinawite (FeS), but were oxidized along the outer margins
of the membrane to green rust, expected to range in compo-
sition from approximately [Fe 4 Fe 2 n (0H) 12 ] 2+ [C0 3 -3H 2 0] 2_
and/or approximately [Fe 3 Fe m (OH) 8 ] 1 [C1.2H 2 0] through to
approximately [Fe 1I Fe II1 (OH) 4 ] 4 [OH] ; to oxidized mackina-
wite containing some Fe m ; then to greigite (approx.
SFeS[Fe 4 S 4 ]SFeS) [100,123,128-131,133-136] or violarite
(approx. SNiS[Fe 2 Ni 2 S 4 ]SNiS) [129,132] associated with minor
clusters of iron-molybdenum sulfide (Mo IV/VI Fe 2 S 5 /2_ ,
Mo 2 v/VI Fe 3 S 9 /2 ~" or Mo^ /VI Fe 5 S?f “) [103-105,121,125]. First,
we turn to the fixation of carbon.

6. The carbon-fixing engine and the role of
electron bifurcators

The electron-donating fuels that were fed continuously to the
compartmental interiors from the alkaline hydrothermal sol-
ution were methane, hydrogen and minor formate, whereas
the potential oxidants in the all-enveloping ocean were carbon
dioxide, nitrate, nitrite, sulfite, native sulfur and ferric iron
[25-27,43-45,54-56,81,90,125,137-141]; cf. [142]. Additional
potential free energy sources were provided by the five units
of pH (equivalent to approx. 300 mV) and the temperature
contrast of around 50-80°C imposed across the mineral barrier
separating the hot alkaline solution from the cool ocean [25,143].
These conditions were maintained over long periods by the
chemical and thermal stability of the hydrothermal system
and the ocean currents, augmented by secondary convection
of ocean water driven by heat in the hydrothermal mound
and its entrainment in the exhaling flow [8]. In cases where
there was a natural narrowing of the mound, the venturi effect
would come into play, autocatalytically sucking the external sol-
utions inwards much in the manner of a carburettor [140].
Flooding of the system was obviated by the precipitation of
further inorganic compartments. Thus, the hydrothermal
mounds were de facto free energy and material capturing devices
that offered a surplus of opportunities for electron bifurcations,
catalysis, reactions, interactions and engine assembly across
those inorganic membranes constituting their outer margins.

rstb.royalsocietypublishing.org Phil Trans R Soc B 368: 20120254

4.4 Ga acidic ocean
~10°C

CCL

pH~5.5

inorganic membranes

Si0 2 , Fe(Ni,Mo)S, green rust |

X filj

aJBJI

pmf-^ 2P ; ->PP ; ^

H + [' 2 <

[Fe n Fe m (OH) 4 ] + [OH]-

''W.Wvl

y

HPO^|

denitrifying

methanotrophic

acetogenesis

CH 3 COOH

‘exhaust’

biosynthesis

electron acceptors (oxidants)
NOj, NOj, Fe 3+

hydrothermal mound
= hatchery of life

■»u

NiFe 5 S g

CH 3 CO~S p

cf. acetyl coA

— no 3 -

electron

bifurcation

^ n ° 2 -

catalyst

Mo IV <->Mo VI

ocean floor

ocean crust

serpentinization produces electron donors in alkaline hydrothermal fluid

Figure 4. Diagram to show how the entropic output from serpentinization fuels an emergent metabolic engine within the concomitantly precipitated alkaline
hydrothermal mound with methane and hydrogen, augmented by pyrophosphate condensation driven by the ambient proton motive force. The natural titration
of the alkaline hydrothermal solution with the acidulous ocean leads to precipitation of chemical garden-like compartments. A secondary acidulous ocean current
bearing the oxidants is convectively driven by heat emanating from the mound and also pulled upward by entrainment in a manner comparable to a carburettor so
that the reductants — delivered at a similar rate to the oxidants — are partially oxidized to organic intermediates [8,26,46]. Reactions are catalysed by the (dis-
located) surfaces of transition metal sulfides or in the interlayers of green rust acting here as a di-iron methane monooxygenase [19,126]. The specific model
engines argued here to have driven the first metabolic pathway are (i) electron bifurcation on Mo-sulfides reduced by H 2 in a two-electron reaction but ejecting
these electrons in a gated manner towards a high potential acceptor (such as nitrate or nitrite) and a low potential iron -nickel -sulfur-containing mineral such as
violarite [19,104,127]. This low potential mineral is considered to achieve reduction of C0 2 to CO in a reaction reminiscent of that at the catalytic metal cluster of C0-
dehydrogenase (CODH); (ii) positive redox feedback loop in the reaction sequence from CH 4 through CH 3 0H to CH 2 0. CH 4 activation towards integration of an oxygen
atom (resulting from NO produced by engine 1 ) requires reducing equivalents which are provided by the (lower midpoint potential) subsequent oxidation step of
CH 3 OH to CH 2 0; (iii) condensation of the two Cl-moieties issued from the high and low potential branches (i) and (ii) into acetate or an acetyl moiety on greigite
[19,46]; (iv) a pyrophosphatase engine comprising green rust interlayers where water activity is close to zero, opens at the oxidized exterior through positive charge
repulsion as the ferrous iron is oxidized (figure 5) [100,101], allowing protons access to the interior which pull orthophosphates by charge attraction (2 x HP0 4 “ or
Pf“) into the subnanometric compartments. Clamped by the ferric iron atoms bordering the walls of the interlayers, neighbouring orthophosphates condense to the
pyrophosphate (which has an overall lower charge as HP 2 07 _ or PPf - ) on interaction with protons. The flux of the remaining protons drives the pyrophosphates
towards the rear exit of the green rust nanocrysts where they phosphorylate organic intermediates produced by engine 1 .

However, the theoretical challenge is to work out how a
metabolism was engineered naturally in this seemingly
appropriate vehicle. We argue that the challenge mainly
amounts to discovering the specific free energy conversion
mechanisms that would have coupled the available sources
of free energy discussed earlier to the production of fixed
carbon. In spite of the obvious difficulties, we do not consider
the quest to be hopeless. After all, these same tensions play
central roles throughout extant life. First of all, in essentially
all cells the generation and use of H + or Na + chemiosmotic
potentials stands at the centre of their energy metabolism.
And, most notably in the present context, the majority of
autotrophic microbes hydrogenate carbon dioxide with the
help of the free energy supplied by either the chemiosmotic
proton or sodium motive force [144-146]. The methanogens
and the homoacetogens, frequently put forward as likely
ancestral types of carbon fixation, manage the hydrogenation
of carbon dioxide through somewhat different formulations
of the acetyl coenzyme-A pathway, both driven in the reduc-
tive direction [147]. Yet, the overall energy available between

the H + /H 2 and the CO 2 /HCOOH couples used by these pro-
karyotes is at the lower limit of viability [46,148]. Moreover,
laboratory experiments involving the reduction of carbon
dioxide in aqueous conditions, even when driven electrochem-
ically, normally stall at formate [149]. Remembering that the
onset of free energy conversion has to conjure with a high
initial threshold of operation [7,150], it therefore seems unli-
kely that the methanogens and the homoacetogens, at least
as they operate today, were the first metabolists when there
was so little redox energy available to them. Given this mar-
ginality, how could comparable pathways to carbon fixation
have arisen and functioned — especially in the absence of
the complex enzymatic and co-factor assistants on which
they now depend?

In response to this question, Nitschke & Russell [46] have
suggested a different way to crank up the first metabolic
engine — one that is driven from either end of the acetyl
CoA pathway, thus obviating the need to assail the steep
endergonic (anti-entropic) gradient to formaldehyde. Fixation
of carbon may have occurred abiotically in single steps

rstb.royalsocietypublishing.org Phil Trans R Soc B 368: 20120254

through the initial generation of two critical reagents, a
(thiolated) methyl group and carbon monoxide, which then
reacted to form acetate. In this scheme, both these intermediate
products are respectively derived from methane and carbon
dioxide through the double use of electron bifurcation
mediated by a molybdenum atom. The redox midpoint poten-
tial of the C0 2 / CO couple is approximately - 700 mV at pH 11,
that is, very likely at best, isopotential with the H 2 -imposed
ambient redox potential in the hydrothermal settings described
earlier. The carbon dioxide conversion to carbon monoxide
would therefore be roughly in thermodynamic equilibrium.
Extant life reduces carbon dioxide to carbon monoxide at a
nickel-containing Fe-S cubane in close proximity to a single
iron atom, the so-called C-cluster (CODH of ACS), which
apparently is sufficiently negative to achieve reduction of
carbon dioxide to carbon monoxide. However, how does this
cluster become reduced in the first place in organisms using
only H 2 as reductant? The concentrations of H 2 as well as
the pH values prevailing around an extant cell would certainly
yield far less reducing power than that found in the hydro-
thermal mound. Nevertheless, life obviously manages to
quantitatively reduce the C-cluster. It has recently been
shown that this redox feat is achieved by electron bifurcation
[151]. As some of us have outlined previously [46,121,125],
electron bifurcation is an entropy-decreasing device par excel-
lence. Although, in extant life, the bifurcating redox centre used
in boosting reducing power to these negative potentials is an
organic molecule, flavin, this role in the mound is likely to
have been played by the two-electron transferring metals mol-
ybdenum or tungsten as argued earlier [121,125]. However,
what may have been the oxidant ultimately necessary to
enable redox bifurcation? Several possible candidates come
to mind such as Fe 3+ , Mn 4+ , sulfur, sulfite or oxidized nitrogen
compounds [25,46,139-142]. Although all of these may have
played a role, we assume that nitrate and nitrite were likely to
have been crucial because they provide both an electron sink
and a source of oxygen for the conversion of methane to metha-
nol as detailed below [139]. The engine 1 in figure 4 therefore
likely was a Mo/W-containing mineral, ratcheting electrons
onto carbon dioxide and driven by the oxidizing potential of
the nitrogen oxyanions, nitrate and/ or nitrite.

Now, carbon monoxide is an extremely reducing molecule
with a redox midpoint potential that was certainly more nega-
tive than that of the mound environment. This spells trouble
because it implies a high tendency to quickly re-dissipate the
temporarily lowered entropy. We assume that this re-dissipa-
tion is prevented, just as in extant life, by the immediate
reaction with a methyl group or methanol molecule derived
from the oxidation of methane and its thiolation [152,153].
The concomitant functioning of both pathways, one reducing
and one oxidizing, therefore is indispensable for stabilizing
the entropy decrease achieved by generating the out-of-
equilibrium carbon monoxide molecule [46]. This brings us to
a seeming contradiction. Although the redox state of carbon,
indeed, becomes more oxidized when going from methane to
methanol, this reaction is more than a simple redox conversion.
In fact, (mildly reducing) electrons are required to activate nitric
oxide molecules, so that an oxygen atom from nitric oxide can
be integrated in the strongly chemically inert methane moiety.
The sum reaction of methane and nitric oxide to yield methanol
and nitrous oxide therefore requires two electrons rather than
providing reducing equivalents. To produce a (volatile) nitric
oxide molecule from nitrite, two more electrons are needed.

From the redox potential of those two reactions (more than
0 mV), H 2 can in principle do the job or at least get the reaction
going. Of course, methane to methanol conversion can also par-
ticipate as oxidant in the bifurcation reaction driving carbon
monoxide production. Methanol in extant life is then oxidized
to formaldehyde, a true oxidation reaction liberating electrons.
Significantly, the reducing power of the liberated electrons is
sufficient to feed the activation of an oxygen atom in the pre-
ceding step from methane to methanol and this is what it
does in extant life. We consider that this positive feedback
coupling of the first two steps in methane oxidation involving
the concomitant reduction of green rust represents another
type of engine lowering the entropy of the system. Formal-
dehyde can then be re-reduced by one electron to yield a
methyl group, presumably attached to a sulfenyl-function.
The methyl will then be condensed with carbon monoxide, fin-
ishing the job of transforming the out of equilibrium carbon
monoxide into the carbon moiety, acetate.

The activated acetate could now provide for biosynthesis.
The methyl sulfide acts here in a similar manner to acetyl
coenzyme-A itself, and the mechanism, while obviating
the need to transit all the intermediates along the acetyl
coenzyme-A pathway, produces a molecular analogue of the
thioester central to much of biochemistry [46,152]. We have
termed this putative first metabolism 'denitrifying methano-
trophic acetogenesis' [46]. Further hydrogenations and
carboxylations of the acetyl thioester, catalysed by iron sul-
fides, could produce the higher carboxylic acids, through
pyruvate to succinate in the incomplete reverse tricarboxylic
acid cycle. And Huber & Wachtershauser [154] have demon-
strated the reductive amination of some of the carboxylic
acids to the corresponding amino acid catalysed by iron mono-
sulfide or ferrous hydroxide, just the fine mineral precipitates
to be found in membranes comprising the outer surfaces of
the hydrothermal mound [122]. Were the thioester to be phos-
phorylated, the activated acetate could now provide for some
of the early bioenergetics as well as for further biosynthesis
[155]. This then brings us to the issue of how the necessary pyr-
ophosphate disequilibrium could be produced abiotically in
the mound's membrane structure.

7. A pyrophosphatase engine: chemiosmosis
for free

Let us first emphasize that we are not here seeking a way to
efficiently condense orthophosphate to pyrophosphate as a
presumed equilibrium reaction (e.g. by catalysis, or raising
the concentration of orthophosphate), but instead a way to
drive this endergonic reaction far from where it would be
at equilibrium. We need this not just, or not primarily, to pro-
duce a sufficiently high concentration of pyrophosphate to
act as a reagent in subsequent reactions, but specifically
to produce a pyrophosphate/orthophosphate disequilibrium
which can then function as a free energy source (not a reactant
source) for driving downstream endergonic reactions — reac-
tions such as the phosphorylation of the thioester mentioned
earlier. But to achieve this, the second law dictates, we need
an FEC engine that can couple the dissipation of some available
free energy source to the anti-entropic production of pyropho-
sphate. If, as seems most likely, we assume that at the
emergence of metabolism the driving disequilibrium for this
process was the geochemically provided proton gradient

rstb.royalsocietypublishing.org Phil Trans R Soc B 368: 20120254

discussed earlier, then we are seeking a mechanism that acts in
similar manner (albeit in reverse) as has recently been proposed
for the membrane-integral K + -dependent H + -pyrophospha-
tase from Vigna radiata [118] and from the homologous
Na + -pyrophosphatase from Thermotoga maritima [119].

The mechanism put forward in these two papers pro-
vides a detailed description of a molecular device that
electromechanically ties the hydrolysis /condensation reaction
inter-converting between pyrophosphate and two orthophos-
phates to the transport of a proton or a sodium ion across
the membrane in which the device is embedded [118,119].
The essential feature of this linkage in condensations is that
it makes each of the two processes conditional on the other —
and with a specific logical directionality, namely, a proton
(or sodium ion) can pass from outside to inside if, and only if,
that happens coincidentally with the condensation and release
of a molecule of pyrophosphate, or conversely, a proton (or
sodium ion) can pass in the opposite direction, if and only if
that happens coincidentally with the hydrolysis of a pyrophos-
phate and the release of the orthophosphate products. Because
of this coupling logic, the device can function as a reversible
free energy converter; converting, for example, the controlled dis-
sipation of an outside-to-inside proton gradient in the production
of a disequilibrium in the concentration of pyrophosphate versus
orthophosphate (i.e. acting as a proton-gradient-driven pyropho-
sphate synthase). Or it can function equally well in reverse as a
proton-pumping pyrophosphatase. Which way it goes depends,
of course, on which way yields a net negative change in free
energy (equivalently a net positive rate of entropy production).

What is most remarkable about the mechanism as pro-
posed by Lin et al. [118] and Kellosalo et al. [119] and also
most important for our present goals, is its stunning simplicity
wherein controllable flexibility is the key device. In particular, a
flexible passageway through the protein can open and expose
an internal cavity alternatively to either side of the membrane
or close it off to both sides. These flexing motions are controlled
by whether charged residues judiciously positioned along
the walls of the passageway are neutralized or not by bind-
ing an appropriate counter-ion involved in the process (e.g. a
proton, or an orthophosphate ion). As proposed, the device
steps sequentially through a series of five configurations, or
states (in the manner analysed at length in such famous treatises
on free energy transduction as those by Caplan & Essig [156]
and by Hill [157]) and translocates one proton and catalyses
one pyrophosphate synthesis (or hydrolysis) per cycle.

This mechanistic simplicity is all the more arresting,
because the device performs an FEC function that is exactly
parallel to that carried out by the rotary ATP-synthases,
which famously stand at the apex of complexity and sophisti-
cation of design as engines of free energy conversion (and
operates much the same way as the Wankel engine [115]).
But it also, quite obviously, makes very much less daunting
the task of finding abiotic versions of a device of this kind in
the mineralogy of the serpentine effluent mounds. We discuss
this issue next and lay our reasons for thinking that the
mineralogy of the membranes formed in the alkaline hydro-
thermal precipitates is a great deal more promising as a
context in which chemiosmotically driven PPi synthase activity
could arise abiotically than one would at first have any reason
to suspect.

When sulfide is present as HS in the alkaline hydrother-
mal solution the inner zones of the precipitated membrane
comprise mackinawite and subordinate greigite nanocrysts.

while the outer zones comprise ferrous hydroxide [123]
which would oxidize in steps, on reaction with nitrate, to
green rust (e.g. approx. [Fe3Fe m (0H) 8 ] + [C1.2H20] _ and
approx. [Fe n Fe m (OH) 4 ] + [OH] _ ) to form a well-ordered, vari-
able valence platy mineral arranged orthogonally to the
membrane outer surface, just as mackinawite tends to be
oriented normal to the inner surface (figure 4) [123,133-136].
The interlayers between these platelets offer subnanometric
compartments in which water activity is vanishingly low. In
a prescient and brilliant paper Arrhenius [100] notes that as
green rust forms, the ferrous hydroxide layers are forced
apart by the ferric ions, admitting counter-ions such as chloride
in the company of water molecules. This layer of water
molecules is clamped between two catalytic surfaces that,
while highly viscous, could permit the persorption of larger
anions such as the di-anion carbonate to replace the chloride
or hydroxide ions in a compartment that still would be less
than a nanometre wide. At relatively low pH, orthophosphate
might be accommodated together with phosphate-charged
reactants between these flexible nanometric membranes
[100,158-160]. These tiny channels have the potential to provide
primitive enzymatic functions. To quote Arrhenius, Tike cells,
they retain phosphate-charged reactants against high concen-
tration gradients and exchange matter with the surroundings
by controlled diffusion through the 'pores' provided by the
opening of the interlayers at the crystal edges. Here, the ex-
posed negative charge on the interrupted metal hydroxide
'membrane' leads to sorption of cations as 'gatekeepers' [100].

The challenge is to imagine how these naturally provided
subnanometric channels might be put to the specific conversion
work that needs to be done. For example, can comparisons be
made with the pyrophosphatases mentioned earlier [118,119]?
These so-called membrane-integral or M-PPases couple
pyrophosphate hydrolysis or synthesis with sodium ion or
proton translocation. The M-PPase has a negatively charged
gate comprising a hinged lysine swinging between an aspartate
and a nearby glutamate residue. The gate can be opened or
closed by a simple binding-change mechanism, and below the
gate is an exit channel. In the case of a putative green rust pyr-
ophosphatase, a possible analogous mechanism might come
about as follows: an initially open, i.e. relatively oxidized, chan-
nel facing the membrane exterior might take up and spatially
confine orthophosphates from the acidulous ocean, partially
neutralizing the local charge configuration within the channel
as it does so and causing the channel to contract locally; this
change might form a gated, active cage, forcing the condensa-
tion of pyrophosphate. As in the case of the protein examples,
this condensation would be expected locally to reduce the over-
all charge, initiating a local positive charge repulsion, and
freeing the pyrophosphate to the interior membrane environ-
ment — with a bias in that direction being ultimately due to
the proton gradient. The newly minted pyrophosphate could
then phosphorylate distal carboxylates of organic molecules
freshly generated on iron-nickel sulfides comprising the
membrane's interior, i.e. in the carbon-fixing engine.

We attempt to make this general model a bit more
specific, and plausible, in the following discussion. As
previously mentioned, green rust of the kind to be precipi-
tated at the interface between the alkaline hydrothermal
solution and acidulous phosphate and iron-bearing ocean
water is likely to comprise [Fe3Fe m (0H) 8 ] + [C1.2H20] _ and
[Fe n Fe m (OH)4] + [OH] _ [161-166]. Officially named fougerite
[163], the mixed valence mineral reacts rapidly and reversibly

rstb.royalsocietypublishing.org Phil Trans R Soc B 368: 20120254

Figure 5. Speculative physical model of a putative green rust (fougerite H + -pyrophosphatase) [cf. 117-119], based on the generation within the mineral inter-
layers of redox polaron 'quasi-particles' — manifest as localized channel dilations — that can propagate in a directed manner along the interlayer. Boundary
conditions are given by the bathing of the outside of the iron hydroxide membrane in an aqueous solution of protons, carbon dioxide, nitrate and ferric iron
(the Hadean Ocean simulant) while the inside, iron sulfide zone of the membrane, is bathed in hydrogen, methane and bisulfide (the alkaline hydrothermal
solution simulant). The transmembrane potential — part redox and part pH gradient — totals approximately 1 V [19,140,148] and provides the vectorial free
energy that drives the system's inherently endergonic processes: (i) the generation and inward propagation of localized, polaron-based, channel dilations, (ii)
the confinement of phosphate under conditions of reduced water activity within a superficially positioned local dilation, (iii) the subsequent condensation to pyr-
ophosphate which in turn permits the mobilization of the polaron dilation and (iv) the 'pumping' of the pyrophosphate into the interior against its own gradient.
The ferrous hydroxide comprising the outer margins of the precipitate membrane begins to be oxidized by nitrate to green rust which has the effect of opening the
interlayers locally as the ferric ions on either side of the interlayer repel each other, the positive charges attracting counter-ions such as chloride, nitrate, carbonate
and phosphate to take up the space [100,101,135,136,163-165]. The changes in local redox state locally distort the crystal structure inducing, via phonon inter-
actions, the formation of localized polaron quasi-particles [171,172]. The polaron-based local dilations produced by the oxidation of green rust migrate through Fe 3+
hole polaron transport, charge hopping interdependently correlating with anion migration along the interlayer towards the interior [173]. The double valent anions
such as orthophosphate (Pi 2- ), confined within localized polaron distorions, are also pushed along the interlayer (acting like a protein channel or pore) which
thereby acts as a peristaltic pump. Condensation of the phosphates to di- or polyphosphates takes place in the confined space of a single polaron dilation positioned
at the external interface within the channel where water activity is low, in a reaction involving one proton and the generation of one water molecule per con-
densation and the consequent lowering of charge, thereby releasing the grip of the electron field and allowing the subsequent release of the condensed phosphates
to the interior [100,108,140,159,171,173-175]. Re-reduction of the same green rust is through the oxidation of the hydrothermal methane and hydrogen (figure 4).

to redox conditions between ferrous (approx. Fe 2 Fe m (OH) 7 )
and ferric fougerite (Fe n Fe 2 n (OH) 8 ) with the obligate intercal-
ation of anions to maintain charge balance [160-165]. Such a
nanocryst may have acted as the pseudo enzyme driving
phosphate condensation in lieu of the membrane helices
[100,165,167-169]. The monovalent interlayer anions drawn
in to balance charge in these varieties of green rust are
more easily exchanged than the divalent ions such as
sulfate and carbonate [165,168], and are thus more suscep-
tible to replacement by active phosphate sorbents [169,170].
We hypothesize that a proton flux, driven by the pH gradient
amounting to five pH units, could translocate the orthophos-
phate anions from the ocean bathing the mound into the
open subnanometric chambers walled by the crystal planes
which tend to be oriented orthogonally to the outer and
inner surface of the membrane (figures 4 and 5). For example,
oxidation of ferrous hydroxide or further oxidation of green
rust by nitrate towards the exterior (ocean side) of the inor-
ganic membrane would have the effect of distorting the
interlayers at their distal ends, opening them up to an
influx of orthophosphate (HPO4 ) from the Hadean Ocean
[176], distortions that, as polarons, would migrate towards
the membrane interior (figure 5). At the same time, the
proton flux might be relied upon to push these counter-
ions down the steep proton gradient into the reduced

interlayer where they would lodge, so blocking the proton
flux [26]. Once contained in these interlayers, the orthophos-
phates are condensed to various pyrophosphate species
such as trimetaphosphate [167,169], with the proximal fer-
rous iron atoms acting in the same role as the five
magnesium ions that neutralize phosphate -phosphate repul-
sion, packed closely around the phosphates in the H + -
pyrophosphatase described by Lin et al. [118]. Such diadochic
substitution has been demonstrated by Athavale et al. [177]
whereby ferrous iron substitutes for magnesium in clamping
phosphates in RNA conformations in the Group I intron P4-
P6 domain of Tetrahymena thermophila. The interlayer water
molecules in the oxidized end-member of fougerite should
permit proton hopping from water molecule to water mol-
ecule via a Grotthuss-type mechanism much as they do in
the exit/entry channel to the extant enzyme [119,178,179].
One of the protons would aid in the condensation in a reac-
tion that also produced a water molecule.

The build up of protons would drive the further conden-
sation of contiguous orthophosphates to the lower-charged
pyrophosphate (HP2O7 ) but at the same time would oxidize
the reduced iron (with the concomitant production of
hydrogen) [137]. The now more oxidized confining walls of
the interlayer would retreat and lose their grip on the pyro-
phosphate so that the activation energy required to drive

rstb.royalsocietypublishing.org Phil Trans R Soc B 368: 20120254

protons down gradient would be substantially lowered
[171,172]. The protons would push the pyrophosphates
through the remaining portion of the interlayer or channel,
releasing them for biosynthetic interactions such as the con-
densation of amino acids to peptides promoted by alkaline
conditions [180-183] (figure 5). This system functions as
an FEC, converting the dissipation of the transmembrane
chemiosmotic disequilibrium into the creation of a pyro-
phosphate chemical disequilibrium on the inside. It
achieves this by making proton translocation and pyrophos-
phate condensation mechanistically gated by, and thus
reciprocally conditional on, each other. This action in turns
depends on the formation of local, redox-driven, polaron-
based structural dilations in the mineral interlayer spaces.
The essential operational logic of the engine is that a proton
cannot pass through the interlayer channel from the exterior
to the interior unless it induces the condensation of phos-
phates taken from the exterior into pyrophosphate, which
action permits proton and pyrophosphate to be driven
together along the interlayer and ultimately released into
the interior. Recharge of the green rust pyrophosphatase
would be from electrons stemming from hydrogen or methane
in the interior which would re-reduce the ferric iron in green
rust resulting in electron hopping towards the exterior until
they reached an unfilled metal site and polarized the neigh-
bouring atoms and generated polarons [171]. Concentrations
of polarons would produce phonons that would act as a
low valence metal [171], distorting the green rust lattice so
that it would regenerate ferrous iron on the green rust inter-
layer walls so that the ensuing orthophosphates would be
re-gripped [173]. Once in a metastable state the redox con-
ditions within the interlayer compartments would oscillate
only within a limited range of ferrous : ferric ratios [162,173].

In this scenario, the translocation of pyrophosphate would
only progress as a second proton is released to the membrane's
interior. The very minimum theoretical H + : PPj ratio thus
would be 2. Surprisingly, just such a 2 : 1 stoichiometry has
been calculated in the operations of H + -pyrophosphatase in
Rhodospirillum rubrum, whereas the H + : ATP ratio is 3.6 in the
same bacterium [184]. Delivered from the green rust in such a
manner the pyrophosphates could phosphorylate thioesters in
further steps to biosynthesis as touched on in §6 on the found-
ing of the acetyl Co A pathway mentioned earlier [24,46,148].
The only experimental support for comparable oligomeri-
zations in mixed-valence double-layer metal hydroxide
minerals has been provided by Pitsch et al. [158] and
Krishnamurthy [185]. They have demonstrated the formation
of tetrose-2,4-diphosphates and hexose-2,4,6-triphosphates
from glycolaldehyde phosphate and pentose-2,4-diphosphates
from glycolaldehyde phosphate and glyceraldehyde-2-phos-
phate, with ribose-2,4-diphosphate formed preferentially to
other pentose-2,4-diphosphates.

8. A tandem of 'mineral' engines to start life?...

The purported redox-controlled phosphorylation outlined
earlier might operate on the same nanometric green rust clus-
ters as the redox changes associated with the oxidation of the
methyl group and its re-reduction with electrons from a mo-
lybdenum cluster. Indeed, supposing these two engines, both
involving green rust and working in concert, were enough to
get a metabolism going within the inorganic compartments.

then a form of vertical reproduction might have led to
ever more complex interactions. The inorganic cells grew,
became sealed, then in response to hydrodynamic pressures,
burst to spawn new contiguous cells. By such a process, any
organic products from one compartment could be fed
forward to the next. Thus, materials generated in the mem-
branes of one cell could be entrained in the flow and born
upward and concentrated in later cells, thereby reducing
the permeability of the membrane as organic molecules,
mainly peptides at first, acted as partial seals [74]. Therefore,
these electrochemical gradients would be dissipated more
effectively and new ones exploited. For example. Dieter
Braun and co-workers [186-188] have demonstrated the
effectiveness of a thermal gradient operating across a compart-
ment's interior in concentrating charged organic molecules
through thermophoresis, and we might imagine a natural elec-
trophoresis sorting and ordering a range of these molecules in
the membrane, the better for their subsequent interactions.
With the drive from these additional engines, in time a Lamark-
ian evolution could, through the emergence of cofactors and a
retroviral-like RNA [189,190], transform to a Darwinian evo-
lution, and new engines approaching those mentioned at the
start of this section could have emerged. And while still in
the mound, perhaps the entire acetyl CoA pathway could
have been sprung, allowing homoacetogens and eventually
methanogens, access to the neighbouring ocean floor and
ocean floor sediments and lava flows, inaugurating the deep
biosphere [191-194].

9. . . .And one-third to see it through to
oxygenic photosynthesis?

At their core, of course, these great transitions are mediated
by the emergence and evolution of new FEC engines.
A newly published study of what is arguably the most conse-
quential of these, the photosystem II (PSII) component of
oxygenic photosynthesis, affords a beautiful insight into
how complex and operationally precise the turnstile mechan-
isms at the heart of biological free energy converters can
become [195]. The PSII engine couples the dissipation of the
free energy of photo-excited electrons — the driving disequi-
librium — to the oxidation (splitting) of water, liberating
protons on the low pH side of the membrane, whereas the
electrons are deployed to provide diffusible reducing equiva-
lents and to take up protons from the high pH side of the
membrane — which outcomes together make up the driven
disequilibrium. The engine's deep challenge, however, is that
it must oxidize two water molecules to produce one mole-
cule of molecular oxygen — while properly dispensing four
charge-separated electron/proton pairs — all in one cycle of
the engine. In the cited study, it is shown that the two-water-
molecule oxidation cycle proceeds through an eight-step
sequence comprising a strictly controlled series of alternating
electron and proton transfers, with each step being conditional
on the completion of its predecessor.

This picture resolves the total cycle into four sequential
instances of a base photon -electron -proton cycle. It is in
this base cycle that the process-locking conditionality require-
ments of FEC in this system are first, and most importantly,
imposed. The key issue is the constraint imposed by the
system on the pathways by which the excited electronic
state created by the absorption of a single photon can be

rstb.royalsocietypublishing.org Phil Trans R Soc B 368: 20120254

relaxed (and the system returned to its photoreceptive initial
condition). Specifically, these constraints make this dissipa-
tive relaxation conditional on the coincident occurrence of
the driven, i.e. endergonic, processes involved in the pro-
ductive transfer of one electron, and then gated by that of
one proton, from the manganese cluster and its surrounds
possibly charged with two water molecules. In this way,
the conversion of the photon's free energy to free energy
stored in the proton gradient and in reduction potential, is
achieved. The cited paper furthermore demonstrates that, as
in the case of the other FEC engines thus far studied in suffi-
cient detail, specific physical movements of the embedding
proteins are apparently required to make the process work.
In the present study, these are resolved as volume changes
(attributable to coulombic effects resulting from shifts in the
local charge configuration) associated in particular with
the steps in the cycle involving proton translocations. It is
finally worth noting in the present context that all of the
charge transfer processes in the PSII cycle are mediated by
a single Mn 4 Ca0 9 catalytic complex comprising a 'distorted
cubane' of structure rather similar to a mineral spinel, just
as ferredoxins, ACS and CODH are comparable to a natural
inverse spinel, inviting the thesis that such mineral structures
were there for the taking from the respective environments by
peptides and proteins as the first metabolists, and sub-
sequently the first oxygenic photosynthesizers emerged
[25,62,63,72-75,196-198]. Oxygenic photosynthesis effected
a qualitative increase in processing by the biosphere at
large [62,63] as the major high potential electron acceptor
oxygen began to make itself felt at the great oxidation event
and the eukaryotic world opened up, eventuating in the
Cambrian and Devonian explosions [199-201].

10. Conclusions

We have attempted in this paper to describe and support a fairly
detailed proposal as to where we need to look, and what we
need to look for, in the attempt to understand how life emerged
on this planet. This proposal traces the story through its physical
and geological provenance, its history, its chemistries and
mineralogy, and its sources of free energy. Finally, we have
described how, in general terms, those sources of free energy
must have become suborned to the support of the necessarily
endergonic processes of pre-life through the action of abiotically
produced mechanisms of free energy conversion. In this story,
we have emphasized that the creation of life is but one piece,
one component of creation, in the great order-creating industry
that is the true business of our dynamic Universe. This order,
whose creation is dictated by the thermodynamics of far-
from-equilibrium systems, is everywhere in the form of auto-
catalytic, work-creating engines — engines which accelerate, as
active devices, the dissipation of the immense astronomy of dis-
equilibrium with which our Universe was bom. And we have
seen how the engines of dissipation created in this way form a
vast hierarchy of wheels within wheels, each wheel an engine
driving engines below it. We have traced the causal, hierarchical
chain of order creation from the galactic-scale wheels of astro-
physics through the planetary wheels of geophysics, on
through the chemical and geochemical micro-scale wheels
that drove directly, we argue, the creation of the wheels of life.
Of course, not all of this picture is yet certain or sharply defined
and many questions remain to be resolved. Most importantly.

perhaps, we cannot yet propose in entirely specific terms test-
able models for how the final wheels in our story would have
arisen and functioned 'abiotically'. But we have suggested a
start that could be made experimentally: the initial geological,
geochemical and electrochemical conditions are relatively well
constrained, the generation of membranes comprising fer-
rous/ferric sulfides and (oxy)hydroxides well attested [123].
The addition, to the experimental model we have previously
investigated, of hydrogen, methane and molybdenum to the
alkaline hydrothermal solution, and nitrate to the carbonic
ocean simulant, may be enough to put the proposed carbon-
fixation and the pyrophosphate engines to trial. These are the
engines that would have allowed the free energy sources (the
disequilibria) vouchsafed to the planet by the geochemistry of
serpentinization operating beneath the Hadean Ocean, to
drive, within the chambers of the porous precipitate mounds
on the ocean floor, the creation of the specific chemical 'order'
which we argue must have arisen for proto-metabolism to
have gotten its start — order in the form of disequilibriated
states of fixed carbon and pyrophosphate. And, in our view,
the goals that must be achieved in this quest now stand before
us in relatively sharp focus.

11. Epilogue

We began this piece with a quote from Boltzmann from 1886 in
which he stated that for 'animate beings' the 'struggle for exist-
ence' is not a struggle for energy but 'a struggle for entropy' [1].
Our choice of this quote reflects our view that the point Boltz-
mann is making is essential to understanding bioenergetics,
and not least to how various disequilibria were harnessed at
the emergence of life. It is unarguable that what Boltzmann
meant by this assertion has long and perfectly passed time's
test — a time, moreover, that has seen a great deal of relevant
and fundamental progress; for example, the development of
non-equilibrium thermodynamics, the understanding of self-
organizing dissipative structures, the chemiosmosis revolution
and the working out of many of the molecular turnstile
mechanisms at the heart of the engines that generate the thermo-
dynamic driving forces of biological systems. However, it seems
to us that Boltzmann's assertion about life and entropy, flowing
directly as it did from his iconic insight about the physical nature
of entropy itself (rightfully regarded as one of the greatest in the
history of science) might today, a century and a quarter later, be
changed slightly to say that what life struggles for is disequili-
bria. For as he well understood and clearly had in mind in his
use of the phrase 'a struggle for entropy', life in fact lives by
the dissipative consumption of thermodynamic disequilibria
and it is through such consumption, suitably enslaved by the
intervening operation of organized engines of disequilibria
conversion, that it generates and maintains the exquisitely
arranged and complexly connected subordinate disequilibria
that make up the necessarily far-from-equilibrium structures
and processes that bring matter to life.

We appreciate help from Jan Amend, Nick Amdt, Laurie Barge,
Giuseppe Etiope, Nigel Goldenfeld, Elizabeth Jagger, Isik Kanik, Richard
Kidd, Nick Lane, Ole Liitjens, Tom McCollom, Shawn McGlynn, Randall
Mielke, James Milner-White, Andrew Russell, Bob Shapiro, Takazo
Shibuya and Lauren White. We also thank Dr Carl Pilcher and the mem-
bers of the NAI-sponsored Thermodynamics Disequilibrium and
Evolution Focus Group for discussions. The research described for this
publication was carried out at the Jet Propulsion Laboratory, California
Institute of Technology, under a contract with the National Aeronautics

rstb.royalsocietypublishing.org Phil Trans R Soc B 368: 20120254

and Space Administration with support by the NASA Astrobiology Insti-
tute (Icy Worlds); at the Institute for Genomic Biology, UIUC with partial
support of the National Aeronautics and Space Administration through
the NASA Astrobiology Institute under Cooperative Agreement No.

NNA13AA91A issued through the Science Mission Directorate, and at
Bioenergetique et Ingenierie des Proteines, CNRS supported by the
French Agence Nationale pour la Recherche (ANR-Blanc-MC2). U.S.
Government sponsorship is acknowledged.

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